SUMMARY

One of the most interesting trade-offs within the vertebrate locomotor
system is that between speed and endurance capacity. However, few studies have
demonstrated a conflict between whole-animal speed and endurance within a
vertebrate species. We investigated the existence of trade-offs between speed
and endurance capacity at both the whole-muscle and whole-animal levels in
post-metamorphs of the frog Xenopus laevis. The burst-swimming
performance of 55 frogs was assessed using a high-speed digital camera, and
their endurance capacity was measured in a constant-velocity swimming
flume.

The work-loop technique was used to assess maximum power production of
whole peroneus muscles at a cycle frequency of 6 Hz, while fatigue-resistance
was determined by recording the decrease in force and net power production
during a set of continuous cycles at 2 Hz. We found no significant
correlations between measures of burst swimming performance and endurance
capacity, suggesting that there is no trade-off between these two measures of
whole-animal performance. In contrast, there was a significant negative
correlation between peak instantaneous power output of the muscles at 6 Hz and
the fatigue-resistance of force production at 2 Hz (other correlations between
power and fatigue were negative but non-significant). Thus, our data support
the suggestion that a physiological conflict between maximum power output and
fatigue resistance exists at the level of vertebrate muscles. The apparent
incongruence between whole-muscle and whole-animal performance warrants
further detailed investigation and may be related to factors influencing both
whole-muscle and whole-animal performance measures.

Introduction

An important research objective within the rapidly expanding discipline of
evolutionary physiology is a more detailed understanding of the role of
physiological constraints in evolution
(Garland and Carter, 1994;
Feder et al., 2000).
Physiological constraints can arise when an organism has to perform multiple
tasks that place conflicting demands on its physiological design: an increase
in the performance of one task may lead to a decrease in the performance of
the other, and an evolutionary trade-off will produce a compromised physiology
that is optimal for neither task. The vertebrate locomotor system is ideal for
studying such performance tradeoffs because the same muscles must often
perform disparate tasks that require conflicting physiological functions.

One well-known and intuitive trade-off within the vertebrate locomotor
system is that between speed and endurance capacity. The intuitive basis of
this performance trade-off probably stems from the observation that elite
specialist sprinting and marathon runners differ substantially in size and
shape, and no athlete excels in both events. Individual differences in the
proportion of fast, powerful muscle fibres to slow more fatigue-resistant
fibres are believed to be the primary physiological basis of this performance
trade-off (Bennett et al.,
1984; Garland,
1988). Consistent with this suggestion, short-distance human
sprinters possess a greater proportion of fast-twitch muscle fibres than do
endurance athletes, and vice versa for the slower more
fatigue-resistant muscle fibres (Komi,
1984; Esbjörnsson et al.,
1993). Similarly, individual differences in the proportions of
different muscle fibre types correlate with differences in locomotor
performance in the lizard Dipsosaurus dorsalis
(Gleeson and Harrison, 1988).
However, only a few studies have demonstrated a conflict between speed and
endurance within a vertebrate species (Dohm
et al., 1996; Reidy et al.,
2000).

Most studies of whole-animal locomotor performance have found either no
correlation or a positive relationship between speed and endurance (e.g.
Ford and Shuttlesworth, 1986;
Garland and Else, 1987;
Garland, 1988; Shaffer et al.,
1989; Tsuji et al., 1989;
Huey et al., 1990;
Jayne and Bennett, 1990;
Sorci et al., 1995). Why these
intraspecific studies have failed to find a trade-off between speed and
endurance, particularly when the physiological mechanism underlying the
trade-off appears to have been identified, is not clear. One possibility is
that the presumed physiological conflict at the level of the muscles is not as
ubiquitous among vertebrates as commonly suggested. Alternatively, the effects
of the physiological conflict at the whole-muscle level may be difficult to
detect at the level of the whole animal. One way of testing these competing
hypotheses is to investigate the existence of trade-offs at different levels
of organisation. The actual site of the speed/endurance trade-off is believed
to be predominantly at the level of the muscles, so investigations of
individual variations in whole-muscle performance may indicate whether the
speed/endurance trade-off should even be expected at the whole-animal
level.

We investigated the existence of trade-offs between speed and endurance
capacity at both the whole-muscle and whole-animal levels in post-metamorphs
of the frog Xenopus laevis. Individual measures of burst swimming
performance and endurance capacity were determined for juvenile X.
laevis, and the work-loop technique was used to determine whether a
conflict exists between maximum power production and fatigue-resistance of
whole muscles. X. laevis are fully aquatic frogs, utilising both
burst swimming for rapid escape from predators and extended bouts of
swimming/jumping during migrations between connected water bodies (or
overland) (Wilson et al.,
2000; Passmore and Carruthers,
1995), so both measures of whole-animal performance appear to be
relevant to their ecology.

Materials and methods

Juvenile Xenopus laevis Daudin at least 6 weeks post-metamorphosis
(size range 0.54-1.98 g) were purchased from a local animal importer in
Antwerp, Belgium. Frogs were returned to the laboratory at the University of
Antwerp, where they were maintained in 201 aquaria at 20 °C until
experiments began. Animals were exposed to a 12h:12h light:dark photoperiod
and were fed frozen worms every second day. After several weeks, the burst
swimming performance and endurance capacity of 55 individuals were assessed.
After the locomotor trials, 18 of the post-metamorphic X. laevis were
transported to the School of Science and the Environment at Coventry
University, England, for analysis of isolated muscle performance using the
work-loop technique.

Locomotor performance

Burst swimming performance was assessed by filming at least five swimming
sequences for each individual with a highspeed digital camera. Swimming
responses were elicited by placing a frog into the centre of a Perspex
swimming arena (0.5 m×0.5 m×0.1 m deep) and tapping its urostyle
with a fine wire probe, usually resulting in 2-3 swimming strokes. Only
responses that produced swimming along the bottom of the aquarium from a
stationary position were analysed. Swimming sequences were filmed by recording
the image at an angle of 90° above the arena with a high-speed digital
camera (Redlake Imaging Corporation, USA) recording at 200 Hz. The
accompanying Redlake software package was used to analyse the startle
responses by playing back the sequences and digitising the tip of the frog's
snout.

Two measures of burst swimming performance were calculated from each
startle response; velocity during leg extension (Umax) and
velocity over an entire stride (Ustr). Velocity over the
leg extension phase was calculated by recording both the time and the distance
moved between the beginning of leg extension (the frame before movement was
first detected) and complete extension of the legs. Stride velocity was
calculated over the entire swimming stroke from the beginning of leg extension
until the end of leg flexion in preparation for the next stroke. The fastest
of the swimming sequences analysed for each individual was used as a measure
of its maximum burst swimming performance. Because there was considerable
variation in the initial position of the hindlegs during the first swimming
stroke of a startle response, only the second swimming stroke was used to
assess maximal performance to ensure that all analysed swimming strokes
started from maximum leg flexion. To assess the repeatability of performance
measures, burst swimming was retested for 26 randomly selected individuals on
the day after initial assessment. Endurance capacity did not differ between
frogs subjected to a single burst swimming trial and those retested the
following day.

Four days after assessment of burst swimming performance, the endurance
capacity of each individual was measured in a Brett-type swimming flume
(Brett, 1964). Endurance
capacity tests were conducted after burst swimming trials to ensure that any
long-term reduction in performance resulting from these more intensive trials
did not influence the burst swimming trials. The flume consisted of a 30 cm
long swimming section of 7 cm diameter through which a continuous water
current was delivered by an adjustable Little Giant water pump (Little Giant,
USA). Immediately prior to assessment of an individual's endurance capacity,
it was placed into the swimming section of the flume and allowed an adjustment
period of 10 min. The water velocity was then increased to 15 cm
s-1, and the frog responded to the continuous water flow by
swimming against the current. The total time taken to reach exhaustion was
recorded for each individual. A manually operated 10 V stimulator grid (Grass
stimulator) was attached to the rear of the swimming section to prevent the
frog from resting during the swimming trial. A 10 ms stimulus was delivered to
the grid when a frog attempted to rest at the rear of the flume, usually
resulting in an immediate return to swimming. We considered an individual had
reached exhaustion when three successive stimuli separated by 1 s failed to
induce a swimming response. Repeatability of endurance was assessed by
retesting 24 randomly selected individuals 2 days after the initial assessment
of endurance.

After locomotor performance trials, morphological measurements were
recorded for each individual; these included mass (with an electronic balance±
0.01 g) and snoutto-vent, femur, tibia and foot length (Mitutoyo
calipers ±0.1 mm).

Isolated muscle performance

The frogs were killed by pithing and transection of the spinal cord, and
the peroneus muscle was removed from the right hindleg and used for the muscle
performance experiments. As we were testing for trade-offs between maximum
power and fatigue resistance at the level of whole muscle, it was imperative
that an appropriate whole muscle was selected. We chose the peroneus muscle
because it was an ideal size for our muscle rig and it was convenient to
dissect. Although not a major muscle involved in locomotion, the peroneus acts
as a knee extensor and is thought to be a power-producing muscle during frog
locomotion (Marsh, 1994). The
peroneus, gastrocnemius and sartorius muscles of Xenopus laevis are
all composed primarily of similar proportions of fast glycolytic fibres
(Putnam and Bennett,
1983).

Dissection was performed at room temperature (20-25 °C) in Ringer's
solution with the following composition (in mmol l-1): NaCl, 115;
KCl, 2.5; Na2HPO4, 2.15; NaH2PO4,
0.85; sodium pyruvate, 5.0; CaCl2, 1.8; pH 7.2 at 20 °C.
Aluminium foil clips were attached to the tendons at the ends of the fibre
bundles and mounted on stainless-steel hooks, with one end attached to a force
transducer (AE 801, SensoNor; force calibration of 150 mN V-1) and
the other to a servomotor (V201, Ling Dynamic Systems). The muscle preparation
was mounted in a temperature-controlled Perspex bath with circulating Ringer's
solution saturated with 100 % oxygen and maintained at a constant
20±0.5 °C.

Stimuli of 2 ms duration were delivered via two parallel platinum
wire electrodes placed on either side of the muscle preparation. A series of
twitches was used to determine the stimulation amplitude and muscle length
(L0) that generated the greatest isometric twitch force. A
train of stimuli was delivered to the muscle to elicit a tetanic contraction.
The frequency of stimulation was adjusted to maximise tetanus height (95-120
Hz) for each muscle and then used in the subsequent work-loop experiments. The
experimental apparatus was controlled and data were collected using the
Testpoint software package (CEC, MA, USA). The data were then exported and
analysed in Microsoft Excel.

Each muscle was then subjected to cycles of oscillatory work, symmetrical
about L0, using the work-loop technique
(Josephson, 1985). A
sinusoidal strain waveform was used during the work-loop experiments because
the in vivo waveform for the peroneus muscle is not known for any
anuran during swimming. The total strain was arbitrarily set at 15 % of
L0, a value that approximates the strain observed for
other anuran hindlimb muscles involved in powering locomotion
(Olson and Marsh, 1998;
Gillis and Biewener, 2000).
Preliminary experiments revealed that the power output of the peroneus muscle
changed with cycle frequency and approached a maximum at around 6 Hz. The
maximum power output of each muscle was therefore measured at a cycle
frequency of 6 Hz. The number of stimuli imposed on the muscle and the timing
of stimulation were adjusted to give maximum power output. A 5 min recovery
period was allowed between each work loop. Control work loops using identical
stimulation parameters were repeated every fourth run to monitor the muscle's
ability to produce power. These control runs showed that muscle power
production did not change by more than 15 % during the measurement of maximum
power output before fatigue runs.

The fatigue-resistance of each muscle was determined by recording the
changes in power production and force during continuous work cycles at 2 Hz.
Observations of whole locomotor performance for the juvenile X.
laevis, whilst assessing endurance capacity, revealed that a realistic
stride frequency approximated 2 Hz. Before a fatigue run, the number of
stimuli and the timing of stimulation were altered to maximise power output at
2 Hz. The fatigue run consisted of 120 cycles of oscillatory work, which
ensured that the power output of all muscles had reached zero. Only one run
was carried out per individual, and the total strain was 15 % of
L0. Preliminary experiments revealed that the net power
production of the muscles during a fatigue run decreased rapidly to zero after
approximately 20-30 cycles. Thus, the fatigue-resistance of power production
for each muscle was estimated by recording the number of cycles required to
reduce power output to 5 % of the initial value. Although maximum force
production for each cycle also decreased rapidly, a performance plateau was
usually reached after approximately 30 cycles. The fatigue-resistance of force
production was therefore estimated by recording the maximum force after 30
cycles as a proportion of the initial value.

At the end of the fatigue runs, the tendons were removed from the muscle,
and excess Ringer's solution was removed by blotting the muscles with
absorbent paper. The wet mass of each muscle was determined with an electronic
balance (A&D Instruments, Oxford, UK) (±0.01 mg) and used to
calculate isometric stress and normalised muscle power output. Morphological
measurements for each frog were recorded using Mitutoyo calipers (Japan)
(±0.01 mm). Muscle cross-sectional area was calculated from muscle mass
and muscle length, with muscle density assumed to be 1060 kg m-3
(Méndez and Keys,
1960).

Statistical analyses

The relationship between body mass and performance parameters was expressed
in the form logy=loga+blogM, where
M is body mass, a is the proportionality coefficient and
b is the mass exponent. Equations were calculated using
log-transformed data and least-squares regression techniques. Pearson's
product moment correlations (rp) were used to examine the
repeatability of whole-animal performance measures between different days.
These correlation analyses were based on the mass residuals of performance
measures when a significant relationship between body mass and performance was
detected. Correlations between measures of whole-animal performance and
whole-muscle performance were carried out on mass residuals (when appropriate;
otherwise, log-transformed raw data were used) using Pearson's product moment
correlation. Negative correlations between measures of speed and endurance
indicate a trade-off in the performance traits. The Bonferroni method was used
for multiple correlative tests by adjusting the significance values
accordingly. Student's t-tests were used to compare measures of
whole-animal endurance capacity between different testing days. All results
are presented as means ± S.E.M. Significance was taken at the level of
P<0.05.

Results

Whole-animal performance

Maximum burst swimming responses typically consisted of two or three
swimming strokes involving rapid extension of the legs from a stationary
crouched position followed by a gliding phase and active leg flexion,
retracting the limbs in preparation for another stroke. For all individuals
combined, Umax was 59.4±1.4 cm s-1 and
Ustr was 48.7±1.4 cm s-1
(N=55). Umax was positively correlated with body
mass and was described by the question
logUmax=1.78+0.20logM (N=55;
r=0.30; P<0.05) (Fig.
1A). In contrast, Ustr was not significantly
influenced by body mass (N=55; r=0.0001;
P>0.05). For both measures of burst swimming, performance was
significantly repeatable across different days (N=26;
Umax, rp=0.57;
Ustr, rp=0.64,
P<0.01).

The mean time taken to reach exhaustion whilst swimming in a
constant-velocity flume was 475±73 s (N=55) on the first day
of testing. Emax was positively correlated with body mass
and was described by the equation
logEmax=2.57+1.4logM (N=55;
r=0.46; P<0.01) (Fig.
1B). Emax differed significantly between
testing days, being more than 40 % lower on the second day of testing
(N=24; day 1, 514.9±119.4 s; day 2, 301.1±44.0 s;
t=-3.35; d.f.=22; P<0.01). Nevertheless, the
Emax of each individual was positively correlated between
testing days (N=24; rp=0.79; P<0.01),
indicating that performance differences among individuals were significantly
repeatable.

Burst swimming speed (either Umax or
Ustr) was not significantly correlated with
Emax (N=55; rp=-0.01;
P=0.94 for Umax; rp=-0.028;
P=0.84 for Ustr), indicating that there was no
trade-off between whole-animal measures of speed and endurance
(Fig. 2). Correlations between
burst swimming speed (either Umax or
Ustr) and Emax based on total limb
length residuals were also non-significant.

Relationship between mass residuals of maximum burst swimming velocity
(Umax) and the time taken to reach exhaustion whilst
swimming at a constant velocity (endurance) for 55 juvenile Xenopus
laevis.

Isolated whole-muscle performance

The mean isometric stress for the peroneus muscle from juvenile Xenopus
laevis was 268±12.7 kN m-2 (N=18). Cycle
frequency affected the peak power output of the peroneus muscle, with values
of 38.7±2.3 W kg-1 at 2 Hz and 71.1±4.0 W
kg-1 (N=18) at 6 Hz. Peak instantaneous power output was
165.7±10.0 W kg-1 at 2 Hz and 257.4±19.4 W
kg-1 (N=18) at 6 Hz. During a typical optimised work loop
at 6 Hz, force began to rise near the end of muscle lengthening and reached a
peak just after maximum muscle length had been reached. Muscle force then
gradually decreased throughout muscle shortening and reached a minimum close
to its shortest length.

During a set of continuous work-loop cycles at 2 Hz, the maximum force
produced during each cycle decreased rapidly over the first 20 cycles and
reached a plateau after approximately 20-30 cycles
(Fig. 3A). The plateau of force
production varied among individuals and was approximately 5-20 % of the force
produced at the start of a fatigue run. Changes in work-loop shape during a
fatigue run reflected both the rapid decrease in force production and the
increase in muscle relaxation time (Fig.
3B). Thus, force generated at peak length and the maintenance of
force during shortening decreased rapidly as the muscle fatigued. When
fatigued, the muscle also failed to relax completely during shortening,
resulting in an increase in force production during muscle lengthening and an
increase in the work required for muscle lengthening. Total power production
decreased rapidly during a set of continuous cycles and usually reached zero
after 20-30 cycles (Fig. 3C).
One of the characteristics of muscle fatigue is its reversibility following a
period of recovery. The maximum power output of peroneus muscle from X.
laevis returned to 78.1±2.3% (N=4) of the pre-fatigue
value after a recovery period of 20 min.

Changes in (A) force, (B) work-loop shape and (C) net power output per
cycle for a representative Xenopus laevis peroneus muscle during a
continuous set of cycles at 2 Hz using the work-loop technique.

Peak instantaneous power output at 6 Hz was negatively correlated with the
fatigue-resistance of force production at 2 Hz (N=18,
rp=-0.58; P<0.01)
(Fig. 4A). Although all other
correlations between measures of power production and fatigue-resistance also
exhibited negative relationships, none was statistically significant
(Fig. 4B-D).

Correlations between measures of maximum power output at 6 Hz and
fatigue-resistance of the peroneus muscle at 2 Hz for 18 juvenile Xenopus
laevis. There was a significant negative correlation between maximum
instantaneous power output and fatigue-resistance of force (% of maximum force
at cycle 30) (A). `Cycles to 5% of maximum power' is the number of cycles
taken to reduce net power to 5% of the initial value at cycle 1. NS,
non-significant Pearson's product moment correlation.

There were no significant correlations between measures of whole-animal
performance and in vitro muscle performance for individual X.
laevis. For example, peak power output and peak instantaneous power
output of the peroneus muscle at 6 Hz were not significantly correlated with
Umax (N=18, rp=0.13;
P>0.05 for peak power output; rp=0.08;
P>0.05 for peak instantaneous power output). In addition, the
fatigue-resistance of force production at 2 Hz was not significantly
correlated with Emax (N=18,
rp=-0.13; P>0.05).

Discussion

The biophysical and biochemical properties of vertebrate skeletal muscle
differ between fast and slow fibre types
(Lannergren and Hoh, 1984;
Gleeson and Harrison, 1986;
Lannergren, 1987;
Esbjörnsson et al., 1993;
Rivero et al., 1993). A
trade-off between speed and endurance capacity should be expected in
vertebrate muscles as a result of this variation in muscle contractile
properties (Bennett et al.,
1984; Garland,
1988). We found evidence of a trade-off between maximum in
vitro power output and fatigue-resistance of whole muscles for
post-metamorphic Xenopus laevis. Peroneus muscles that produced high
levels of in vitro mechanical power generally possessed lower
fatigue-resistance than muscles producing low levels of mechanical power.
Thus, our data support the suggestion that a physiological conflict between
maximum power output and fatigue-resistance exists at the level of the
muscles. Although most correlations between measures of power output and
fatigue-resistance of whole muscles were non-significant, all demonstrated
negative correlations.

Comparisons of mechanical properties of the peroneus with those reported
previously are difficult because of its limited use for studies of muscle
mechanics. However, its general structure appears to be similar to that of the
gastrocnemius and sartorius muscles
(Putnam and Bennett, 1983),
which have been well studied for numerous anurans (for a review, see
Marsh, 1994). In our study,
mean maximum isometric stress for peroneus muscles was comparable both with
that of X. laevis sartorius at 20 °C (mean maximum stress of 215
kN m-2) (Altringham et al.,
1996) and with the range of previous values for anuran muscles at
20 °C (Marsh, 1994).
Maximum power outputs for X. laevis peroneus muscle at 6 Hz are also
similar to those recorded for X. laevis sartorius from similar-sized
individuals (Altringham et al.,
1996). Fatigue-induced changes in the mechanical properties of
X. laevis peroneus muscle were almost completely reversible, with
in vitro performance returning to approximately 80% of pre-fatigue
values within 20 min. Decreases in power output during a fatigue run were due
to a reduction in force production and to an increase in relaxation time.
Although few studies have investigated the fatigue-induced changes in
contractile properties during sinusoidal work, all report that force
production and relaxation rate changed simultaneously during fatigue
(Syme and Stevens, 1989;
Stevens and Syme, 1993;
Askew and Marsh, 1997).

We found no correlation between measures of maximum burst swimming speed
and endurance capacity for juvenile X. laevis, suggesting that no
trade-off exists between these two performance measures at the whole-animal
level. Most other intraspecific studies of whole-animal performance also
report no trade-off between whole-animal measures of speed and endurance
capacity (e.g. Bennett, 1980;
Ford and Shuttlesworth, 1986;
Garland and Else, 1987;
Garland, 1988,
1994;
Tsuji et al., 1989;
Huey et al., 1990;
Jayne and Bennett, 1990;
Secor et al., 1992;
Sorci et al., 1995). Empirical
support for the speed/endurance trade-off at the whole-animal level comes from
only a few intra- and inter-specific studies. Reidy et al.
(2000) found a negative
correlation between a measure of burst swimming performance and endurance
capacity in the Atlantic cod (Gadus morhua). In a recent
interspecific phylogenetic study of lizard locomotion, Vanhooydonck et al.
(2001) reported a trade-off
between speed and endurance among several species of lacertid lizard. In a
quantitative genetic analysis of sprinting and endurance capacity in the
laboratory house mouse (Mus domesticus), Dohm et al.
(1996) found a negative genetic
correlation between sprint running and swimming endurance.

The absence of a speed/endurance trade-off for post-metamorphic X.
laevis at the level of the whole animal, even though it was detected at
the level of the whole muscles, suggests an apparent incongruence between
whole-animal and whole-muscle performance. Assuming that the physiological
conflict identified for the peroneus muscle also occurs in other larger
muscles that have a greater direct influence on locomotor performance, then
whole-animal performance should reflect the trade-offs imposed on the muscular
system. Several alternative hypotheses relating to the robustness of the
whole-muscle and whole-animal analyses, and factors masking a possible
trade-off at the whole-animal level, may help explain this apparent mismatch
between whole-animal and whole-muscle performance.

Muscles in vivo are used in dynamic and complex ways, so it is
possible that the in vitro measures of muscle performance do not
adequately reflect the in vivo locomotor state. Compared with
whole-animal measures of endurance, in vitro fatigue of force and
power production for the peroneus muscles of juvenile X. laevis
occurred rapidly. The mean number of swimming strides before exhaustion was
more than 800, while for most whole peroneus muscles power output decreased to
zero within 30 cycles. During an in vitro fatigue experiment, muscle
stimulation parameters were set to elicit maximum power production for
non-fatigued muscle and presumably recruited all fibres in each cycle. In
contrast, not all the muscle fibres are simultaneously recruited in
vivo during extended bouts of locomotion, with muscle fibres alternating
between rest and work. Thus, it is possible that our in vitro
measures of muscle performance do not relate to the in vivo locomotor
conditions. Future studies of muscle fatigue may benefit from replicating the
cycling of muscle fibre activation by alternating passive and active
stimulation loops during a fatigue run, thereby more closely representing
in vivo muscle fatigue.

The impact of motivation and other behavioural effects on whole-animal
measures of locomotor performance is more difficult to quantify. It is
possible that the measures of locomotor performance used in this study do not
adequately determine the actual maximum locomotor capabilities of each
individual frog. This is a potential problem facing all researchers studying
whole-animal performance. Although measures of X. laevis performance
were repeatable for individuals across different days, it is still possible
that much of this inter-individual variability is attributable to underlying
motivational/behavioural rather than physiological/morphological variation.
This seems especially likely for measures of endurance capacity for X.
laevis, which displayed great inter-individual variation (100-2000 s to
reach exhaustion). Coefficients of variation differed substantially between
measures of endurance (approximately 115 %) and burst swimming performance
(approximately 20 %). Such large inter-individual variation may be due to
motivational or general behavioural differences rather than to underlying
physiological determinants of performance.

Other physiological or behavioural factors besides muscular performance may
also be masking the speed/endurance trade-off at the whole-animal level.
Several recent studies examining the physiological basis of avian locomotor
physiology suggest that factors other than muscular performance (e.g. the mass
of central organs) may be more important determinants of whole-animal aerobic
performance (Chappell et al.,
1999; Hammond et al.,
2000). Individual variation in endurance capacity caused by other
physiological factors may require very large sample sizes to detect
muscle-mediated trade-offs at the whole-animal level. Even more problematic
are factors, such as general health and condition, prior injury or motivation,
that may result in positive correlations between different whole-animal
performance traits and effectively swamp more subtle muscle-mediated
trade-offs within an individual. Several recent studies of locomotion have
also emphasised that most organisms use a more intermittent type of locomotion
during extended bouts of movement rather than the steady-state type most
commonly examined (for a review, see
Kramer and McLaughlin, 2001).
Both the whole-muscle and the whole-animal measures of endurance capacity used
in our study are based on a steady-state type of locomotion and fatigue,
possibly questioning the ecological relevance of the performance measures
studied.

For the juvenile X. laevis, we found no correlation between
whole-animal measures of performance and whole-muscle performance for any
variables. The absence of correlation between different levels of organisation
may indicate that the traits measured are not important determinants of
performance or that measures of whole-animal performance are not adequate
estimates of locomotor capacities. However, given that the mass of the
peroneus muscle of X. laevis is very small in comparison with the
total muscle mass used during locomotion, a correlation between whole animal
and whole muscle is unlikely. Studies investigating the physiological
determinants of locomotor performance in vertebrates have experienced mixed
results. Although several studies have found correlations between individual
variation in locomotor or aerobic performance and a variety of physiological
processes (Garland, 1984;
Bennett et al., 1989;
Kolok, 1992;
Chappell et al., 1999;
Garenc et al., 1999;
Hammond et al., 2000), just as
many have found either no correlation or only for a particular sex or life
history stage (Garland, 1984;
Kolok and Farrell, 1994;
Garland et al., 1995;
Garenc et al., 1999;
Hammond et al., 2000).

In the present study, we found evidence of a trade-off between maximum
power output and the fatigue-resistance of whole muscles for Xenopus
laevis. In contrast, we found no correlation between whole-animal
measures of speed and endurance capacity. This apparent incongruence between
different levels of analysis may be due to several factors affecting both
whole-muscle and whole-animal performance measures and warrants further
detailed investigation.

ACKNOWLEDGEMENTS

We thank Iain Young and Graham Askew for their advice in producing the
work-loop apparatus and assistance in programming Testpoint, Michael Jollie
and Ken Smith for building the work-loop apparatus and Goedren De Boek for the
use of the swimming flume. We also thank Jan Scholliers, Mark Bodycote, Adrian
Wallen and Jen McKain for technical assistance. This research was supported by
a GOA-BOF project (University of Antwerp 1999-2003) awarded to R.V.D. and a
Royal Society Grant awarded to R.S.J.

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Social insects are excellent models for studying phenotypic plasticity. Beryl Jones and Gene Robinsonreview issues associated with understanding the genetics of plasticity-first evolution and outline an empirical approach to help advance this field.

JEB at SICB 2019

If you’re going to the SICB annual meeting in Tampa from 3 to 7 January, call by Booth #313 to chat to JEB Reviews Editor Charlotte Rutledge and pick up the new JEB T shirt and 2019 calendar, and other JEB goodies!

Did you know The Company of Biologists invites applications from the organisers of a range of charitable activities, including meetings, workshops and conferences, in the fields covered by our journals? The next deadline for grant applications is 4 January.

Rasmus Ernhighlights a recent preprint from Takuya Sato and colleagues that investigates the effects of predation pressure and resource abundance on foraging behaviour of fish in social dominance hierarchies.